Interaction of hematopoietic progenitor kinase 1 with adapter proteins Crk and CrkL leads to synergistic activation of c-Jun N-terminal kinase

Molecular and Cellular Biology

Volumn 19, Issue 2, 1999, Pages 1359-1368

  Ling, Pin ^a   Yao, Zhengbin ^b   Meyer, Christian F ^a   Wang, Xuhong Sunny ^b   Oehrl, Wolf ^c   Feller, Stephan M ^c   Tan, Tse Hua ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b AMGEN INC   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PHOSPHOAMINO ACID; PHOSPHOTRANSFERASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL CULTURE; CELL LYSATE; DENSITOMETRY; ENZYME ACTIVITY; HEMATOPOIETIC SYSTEM; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 0032930551     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.2.1359     Document Type: Article

References (67)

1. Anafi, M., F. Kiefer, G. D. Gish, G. Mbamalu, N. N. Iscove, and T. Pawson. 1997. SH2/SH3 adaptor proteins can link tyrosine kinases to a Ste20-related protein kinase, HPK1. J. Biol. Chem. 272:27804-27811.
2. Birge, R. B., J. E. Fajardo, B. J. Mayer, and H. Hanafusa. 1992. Tyrosine-phosphorylated epidermal growth factor receptor and cellular p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J. Biol. Chem. 267:10588-10595.
3. Boussiotis, V. A., G. J. Freeman, A. Berezovskaya, D. L. Barber, and L. M. Nadler. 1997. Maintenance of human T cell anergy: blocking of IL-2 gene transcription by activated Rap1. Science 278:124-128.
4. Buday, L., A. Khwaja, S. Sipeki, A. Farago, and J. Downward. 1996. Interactions of Cbl with two adapter proteins, Grb2 and Crk, upon T cell activation. J. Biol. Chem. 271:6159-6163.
5. Burridge, K., C. E. Turner, and L. H. Romer. 1992. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119:893-903.
6. Chen, Y.-R., X. Wang, D. Templeton, R. J. Davis, and T.-H. Tan. 1996. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation: duration of JNK activation may determine cell death and proliferation. J. Biol. Chem. 271:31929-31936.
7. Cohen, G. B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80:237-248.
8. Crabtree, G. R. 1989. Contingent genetic regulatory events in T lymphocyte activation. Science 243:355-361.
9. Derijard, B., M. Hibi, I.-H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
10. Derijard, B., J. Raingeaud, T. Barrett, I.-H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682-685.
11. Diener, K., X. S. Wang, C. Chen, C. F. Meyer, J. Bray, M. Zukowski, T.-H. Tan, and Z. Yao. 1997. Activation of the c-Jun N-terminal kinase pathway by a novel protein kinase related to human germinal center kinase. Proc. Natl. Acad. Sci. USA 94:9687-9692.
12. Feller, S. M., B. Knudsen, and H. Hanafusa. 1994. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13:2341-2351.
13. Feller, S. M., B. Knudsen, and H. Hanafusa. 1995. Cellular proteins binding to the first homology 3 (SH3) domain of the proto-oncogene product c-Crk indicate Crk-specific signaling pathways. Oncogene 10:1465-1473.
14. a. Feller, S.M., G. Posern, J. Voss, C. Kardinal, D. Sakkab, J. Zheng, and B. Knudsen. 1998. Physiological signals and oncogenesis mediated through Crk family adaptor proteins. J. Cell. Physiol. 177:535-552.
15. Galcheva-Gargova, Z., B. Derijard, I.-H. Wu, and R. Davis. 1994. An osmosensing signal transduction pathway in mammalian cells. Science 265:806-808.
16. Hu, M. C.-T., W. R. Qiu, X. Wang, C. F. Meyer, and T.-H. Tan. 1996. Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev. 10:2251-2264.
17. Ip, Y. T., and R. J. Davis. 1998. Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr. Opin. Cell Biol. 10:205-219.
18. Kiefer, F., L. Tibbles, A. M. Anafi, A. Janssen, B. W. Zanke, N. Lassam, T. Pawson, J. R. Woodgett, and N. N. Iscove. 1996. HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J. 15:7013-7025.
19. Knudsen, B. S., J. Zheng, S. M. Feller, J. P. Mayer, S. K. Burrell, D. Cowburn, and H. Hanafusa. 1995. Affinity and specificity requirements for the first Src homology 3 domain of the Crk proteins. EMBO J. 14:2191-2198.
20. Lai, J.-H., G. Hovath, J. Subleski, J. Bruder, P. Ghosh, and T.-H. Tan. 1995. RelA is a potent transcriptional activator of the CD28 response element within the interleukin-2 promoter. Mol. Cell. Biol. 15:4260-4271.
21. Lin, A., A. Minden, H. Martinetto, F.-X. Claret, C. Lange-Carter, F. Mercurio, G. L. Johnson, and M. Karin. 1995. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268:286-290.
22. Marengere, L. E., C. Mirtsos, I. Kozieradzki, A. Veillette, T. W. Mak, and J. M. Penninger. 1997. Proto-oncoprotein Vav interacts with c-Cbl in activated thymocytes and peripheral T cells. J. Immunol. 159:70-76.
23. Margolis, B., O. Silvennoinen, F. Comoglio, C. Roonprapunt, E. Skolnik, A. Ullrich, and J. Schlessinger. 1992. High-efficiency expression/cloning of epidermal growth factor-receptor-binding proteins with Src homology 2 domains. Proc. Natl. Acad. Sci. USA 89:8894-8898.
24. Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495-5500.
25. Matsuda, M., and T. Kurata. 1996. Emerging components of the Crk oncogene product: the first identified adaptor protein. Cell. Signalling 8:335-340.
26. Matsuda, M., S. Tanaka, S. Nagata, A. Kojima, T. Kurata, and M. Shibuya. 1992. Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell. Biol. 12:3482-3489.
27. Mayer, B. J., M. Hamaguchi, and H. Hanafusa. 1988. A novel viral oncogene with structural similarity to phospholipase C. Nature 332:272-275.
28. Mayer, B. J., and H. Hanafusa. 1990. Association of the v-crk oncogene product with phosphotyrosine-containing proteins and protein kinase activity. Proc. Natl. Acad. Sci. USA 87:2638-2642.
29. Minden, A., and M. Karin. 1997. Regulation and function of the JNK subgroup of MAP kinases. Biochim. Biophys. Acta 1333:85-104.
30. Minden, A., A. Lin, F.-X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcription activity by the small GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
31. Minden, A., A. Lin, T. Smeal, B. Derijard, M. Cobb, R. Davis, and M. Karin. 1994. c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol. Cell. Biol. 14:6683-6688.
32. Muegge, K., T. M. Williams, J. Kant, M. Karin, R. Chiu, A. Schmidt, U. Siebenlist, H. A. Young, and S. K. Durum. 1989. Interleukin-1 costimulatory activity on the interleukin-2 promoter via AP-1. Science 246:249-251.
33. Nichols, G., M. Raines, J. Vera, L. Lacomis, P. Tempst, and D. Golde. 1994. Identification of CRKL as the constitutively phosphorylated 39-kD tyrosine phosphoprotein in chronic myelogenous leukemia cells. Blood 84:2912-2918.
34. Northrop, J. P., K. S. Ullman, and G. R. Crabtree. 1993. Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells (NF-AT) complex. J. Biol. Chem. 268:2917-2923.
35. Oda, T., C. Heaney, J. Hagopian, K. Okuda, J. Griffin, and B. Druker. 1994. Crk1 is the major tyrosine-phosphorylated protein in neutrophils from patients with chronic myelogenous leukemia. J. Biol. Chem. 269:22925-22928.
36. Pawson, T. 1995. Protein modules and signalling networks. Nature 373:573-580.
37. Pombo, C. M., J. H. Kehrl, S. Irma, J. R. Woodgett, T. Force, and J. M. Kyriakis. 1995. Activation of the SAPK pathway by the human STE20 homogoeu germinal centre kinase. Nature 377:750-754.
38. Reichman, C., B. Mayer, S. Keshav, and H. Hanafusa. 1992. The product of the cellular crk gene consists primarily of SH2 and SH3 regions. Cell Growth Differ. 3:451-460.
39. Ren, R., Z. S. Ye, and D. Baltimore. 1994. Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev. 8:783-795.
40. Salmeron, A., T. B. Ahmad, G. W. Carlile, D. Pappin, R. P. Narsimhan, and S. C. Ley. 1996. Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncogene, a novel MAP kinase kinase kinase. EMBO J. 15:817-826.
41. Sanchez, I., R. T. Hughes, B. J. Mayer, K. Yee, J. R. Woodgett, J. Avruch, J. M. Kyriakis, and L. I. Zon. 1994. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature 372: 794-798.
42. Sawasdikosol, S., J. H. Chang, J. C. Pratt, G. Wolf, S. E. Shoelson, and S. J. Burakoff. 1996. Tyrosine-phosphorylated Cbl binds to Crk after T cell activation. J. Immunol. 157:110-116.
43. Schaller, M. D., and J. T. Parsons. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15:2635-2645.
44. Schwartz, R. H. 1992. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 71:1065-1068.
45. Senechal, K., J. Halpern, and C. L. Sawyers. 1996. The CRKL adaptor protein transforms fibroblasts and functions in transformation by the BCR-ABL oncogene. J. Biol. Chem. 271:23255-23261.
46. Senechal, K., C. Heaney, B. Druker, and C. L. Sawyers. 1998. Structural requirements for function of the Crk1 adapter protein in fibroblasts and hematopoietic cells. Mol. Cell. Biol. 18:5082-5090.
47. Serfling, E., R. Barthelmas, I. Pfeuffer, B. Schenk, S. Zarius, R. Swoboda, F. Mercurio, and M. Karin. 1989. Ubiquitous and lymphocyte-specific factors are involved in the induction of the mouse interleukin 2 gene in T lymphocytes. EMBO J. 8:465-473.
48. Sluss, H. K., T. Barrett, B. Derijard, and R. J. Davis. 1994. Signal transduction by tumor necrosis factor mediated by JNK protein kinases. Mol. Cell. Biol. 14:8376-8384.
49. Sparks, A. B., J. E. Rider, N. G. Hoffman, D. M. Fowlkes, L. A. Quilliam, and B. K. Kay. 1996. Distinct ligand preferences of Src homology 3 domains from Src, Yes, Abl, Cortactin, p53bp2, PLCγ, Crk, and Grb2. Proc. Natl. Acad. Sci. USA 93:1540-1544.
50. Su, B., E. Jacinto, M. Hibi, T. Kallunki, M. Karin, and Y. Ben-Neriah. 1994 JNK is involved in siganl integration during costimulation of T lymphocytes. Cell 77:727-736.
51. Su, Y.-C., J. Han, S. Xu, M. Cobb, and E. Y. Skolnik. 1997 NIK is a new Ste20-related kinase that binds NCK and MEKK1 and activates the SAPK/JNK cascade via a conserved regulatory domain. EMBO J. 16:1279-1290.
52. Tanaka, M., R. Gupta, and B. J. Mayer. 1995. Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol. Cell. Biol. 15:6829-6837.
53. Tanaka, S., T. Morishita, Y. Hashimoto, S. Hattori, S. Nakamura, M. Shibuya, K. Matuoka, T. Takenawa, T. Kurata, and K. Nagashima. 1994. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91:3443-3447.
54. Tanaka, S., T. Ouchi, and H. Hanafusa. 1997. Downstream of Crk adaptor signaling pathways: activation of Jun kinase by v-Crk through the guanine nucleotide exchange protein C3G. Proc. Natl. Acad. Sci. USA 94:2356-2361.
55. ten Hoeve, J., V. Kaartinen, T. Fioretos, J. Voncken, N. Heisterkamp, and J. Groffen. 1994. Cellular interactions of CRKL, and SH2-SH3 adaptor protein. Cancer Res. 54:2563-2567.
56. ten Hoeve, J., C. Morris, N. Heisterkamp, and J. Groffen. 1993. Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene 8:2469-2474.
57. Teramoto, H., O. A. Coso, H. Miyata, T. Igishi, T. Miki, and J. S. Gutkind. 1996. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway: a role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J. Biol. Chem. 271:27225-27228.
58. 2-terminal kinase. Proc. Natl. Acad. Sci. USA 94:7337-7342.
59. Tung, R.M., and J. Blenis. 1997. A novel human SPS1/STE20 homologue, KHS, activates Jun N-terminal kinase. Oncogene 14:653-659.
60. Ullman, K. S., J. P. Northrop, A. Admon, and G. R. Crabtree. 1993. Jun family members are controlled by a calcium-regulated, cyclosporin A-sensitive signaling pathway in activated T lymphocytes. Genes Dev. 7:188-196.
61. Wang, W., G. Zhou, M. C.-T. Hu, Z. Yao, and T.-H. Tan. 1997. Activation of the hematopoietic progenitor kinase-1 (HPK1)-dependent, stress-activated c-Jun N-terminal kinase (JNK) pathway by transforming growth factor β (TGF-β)-activated kinase (TAK1 ), a kinase mediator of TGF-β signal transduction. J. Biol. Chem. 272:22771-22775.
62. Whitmarsh, A. J., J. Cavanagh, C. Tournier, J. Yasuda, and R. J. Davis. 1998. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671-1674.
63. Whitmarsh, A. J., and R. J. Davis. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. 74:589-607.
64. 2-terminal kinase-specific kinase. Mol. Cell. Biol. 17:7407-7416.
65. Yao, Z., K. Diener, X. S. Wang, M. Zukowski, G. Matsumoto, G. Zhou, L. A. Tibbles, T. Sasaki, H. Nishina, T.-H. Tan, J. Woodgett, and J. M. Penninger. 1997. Activation of stress-activated protein kinase/c-Jun N-terminal protein by a novel mitogen-activated protein kinase kinase (MKK7). J. Biol. Chem. 272:32378-32383.
66. Yao, Z., G. Zhou, X.S. Wang, A. Brown, K. Diener, H. Gan, and T.-H. Tan. A novel human STE20-related protein, HGK, that specifically activates the JNK signaling pathway. J. Biol. Chem., in press.
67. Yu, H., J. K. Chen, S. Feng, D. C. Dalgarno, A. W. Brauer, and S. L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76:933-945.